Sources of Infant Pertussis Infection inthe United StatesTami H. Skoff, MSa, Cynthia Kenyon, MPHb, Noelle Cocoros, DSc, MPHc, Juventila Liko, MD, MPHd, Lisa Miller, MD, MSPHe,Kathy Kudish, DVM, MSPHf, Joan Baumbach, MD, MPH, MSg, Shelley Zansky, PhDh, Amanda Faulkner, MPHa, Stacey W. Martin, MSca

abstractBACKGROUND: Pertussis is poorly controlled, with the highest rates of morbidity and mortalityamong infants. Although the source of infant pertussis is often unknown, when identified,mothers have historically been the most common reservoir of transmission. Despite highvaccination coverage, disease incidence has been increasing. We examined whether infantsource of infection (SOI) has changed in the United States in light of the changing epidemiology.

METHODS: Cases,1 year old were identified at Enhanced Pertussis Surveillance sites between January1, 2006 to December 31, 2013. SOI was collected during patient interview and was defined asa suspected pertussis case in contact with the infant case 7 to 20 days before infant cough onset.

RESULTS:A total of 1306 infant cases were identified; 24.2%were,2months old. An SOI was identifiedfor 569 cases. Infants 0 to 1 months old were more likely to have an SOI identified than 2- to 11-month-olds (54.1% vs 40.2%, respectively; P, .0001). More than 66% of SOIs were immediate familymembers, most commonly siblings (35.5%), mothers (20.6%), and fathers (10.0%); motherspredominated until the transition to siblings beginning in 2008. Overall, the SOI median age was14 years (range: 0–74 years); median age for sibling SOIs was 8 years.

CONCLUSIONS: In contrast to previous studies, our data suggest that the most common source oftransmission to infants is now siblings. While continued monitoring of SOIs will optimizepertussis prevention strategies, recommendations for vaccination during pregnancy shoulddirectly increase protection of infants, regardless of SOI.

WHAT’S KNOWN ON THIS SUBJECT: The source ofinfant pertussis infection is typically identified∼50% of the time. Historically, mothers havebeen identified as the most common source ofpertussis transmission to infants.

WHAT THIS STUDY ADDS: This analysis of 8 yearsof enhanced pertussis surveillance data hasuncovered a shift in the most common source ofinfant pertussis infection in the United Statesfrom mothers to siblings.

aCenters for Disease Control and Prevention, Atlanta, Georgia; bMinnesota Department of Health, St Paul,Minnesota; cDepartment of Population Medicine, Harvard Medical School and Harvard Pilgrim HealthcareInstitute, Boston, Massachusetts; dPublic Health Division, Oregon Health Authority Portland, Oregon; eColoradoDepartment of Public Health and Environment, Denver, Colorado; fConnecticut Department of Public Health,Hartford, Connecticut; gNew Mexico Department of Health, Santa Fe, New Mexico; and hNew York StateDepartment of Health, Albany, New York

Ms Skoff conceptualized and designed the analysis, supervised data collection at participating sites,carried out the initial and subsequent analyses, and drafted the initial manuscript; Ms Kenyon, Liko, andKudish and Drs Cocoros, Miller, Baumbach, and Zansky contributed to the design of the analysis,supervised and participated in data collection at participating sites, contributed to interpretation of data,and provided critical review of the manuscript for important intellectual content; Ms Faulkner contributedto the design of the analysis; supervised data collection at the participating sites; contributed to theanalysis, cleaning, and interpretation of data; and provided critical review of the manuscript forimportant intellectual content; Ms Martin contributed to the design of the analysis, provided supervisionin the analysis and interpretation of data, and provided critical review of the manuscript for importantintellectual content; and all authors approved the final manuscript as submitted.

The findings and conclusions in this review are those of the authors and do not necessarilyrepresent the official position of the Centers for Disease Control and Prevention.

www.pediatrics.org/cgi/doi/10.1542/peds.2015-1120

DOI: 10.1542/peds.2015-1120

Accepted for publication Jul 14, 2015

Address correspondence to Tami H. Skoff, MS, Centers for Disease Control and Prevention, 1600Clifton Rd, Atlanta, GA 30329. E-mail: tlh9@cdc.gov

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Pertussis is a highly contagious,vaccine-preventable disease withsecondary attack rates reaching ashigh as 80% in susceptibleindividuals.1 Pertussis vaccines areincluded as part of routine childhoodimmunizations in the United Statesand are currently recommended asa 5-dose series for infants and youngchildren.2 Because these vaccines donot confer lifelong immunity,reduced-dose acellular pertussisvaccines combined with tetanus anddiphtheria toxoids (Tdap) wereintroduced in the United States in2005 for routine use as a singlebooster dose among adolescents andadults.3,4 Despite high or increasingcoverage with pertussis vaccines, theincidence of disease has been slowlyincreasing in a number of countrieswith notable epidemic peaks in recentyears. The epidemiology of pertussishas also evolved, with a growingburden of disease among recentlyvaccinated children and adolescents.5

This trend is particularly evident incountries that have replaced whole-cellvaccine formulations with acellularpertussis vaccines (aP); the transitionfrom whole-cell vaccine to aP vaccinesin the United States occurred duringthe 1990s. Waning immunity incohorts that received aP vaccines fortheir childhood series has been well-documented in recent studies.6–12

Infants are at greatest risk for diseaseand death from pertussis, especiallyduring the first 2 months of life beforepertussis immunizations begin.Numerous studies have evaluated thesource of pertussis transmission toinfants and typically report anunknown source of infection for$50% of infant cases.13–15 Whena source is identified, mothers havebeen the most commonly cited sourceof infection in the United States(32%–37%).13,15 However, recentlypublished data from Australia and theNetherlands suggest that siblings areplaying an increasingly important rolein the transmission of pertussis toyoung infants in these countries.16–18

The objective of this evaluation wasto use Enhanced PertussisSurveillance (EPS) data collectedbetween 2006 and 2013 to identifythe most common sources of infantpertussis infections in the UnitedStates and identify any changes intransmission of disease to infants inlight of the shifting epidemiology.

METHODS

Surveillance

Cases of pertussis were identifiedthrough Enhanced PertussisSurveillance in 7 states betweenJanuary 1, 2006, and December 31,2013. The surveillance area and datesof participation varied by state andincluded Colorado (5-county Denvermetropolitan area; January 1,2011–December 31, 2013),Connecticut (statewide; January 1,2011–December 31, 2013),Massachusetts (statewide; January 1,2006– December 31, 2010),Minnesota (statewide; January 1,2006–December 31, 2013), NewMexico (statewide; January 1,2011–December 31, 2013), New York(15-county Rochester and Albanyareas; January 1, 2011–December 31,2013), and Oregon (3-countyPortland metropolitan area; January1, 2010–December 31, 2013). EPSbecame part of the EmergingInfections Program Network in 2011and is characterized by improvedcompleteness and quality of pertussissurveillance data and augmented datacollection that surpasses what iscurrently reported through theNational Notifiable DiseasesSurveillance System (NNDSS). As partof EPS, pertussis cases are reported tolocal or state health departments byclinical or reference laboratories aftera positive laboratory result. Usinginformation obtained from the case’sdiagnosing health care provider andthrough case-patient interview, publichealth surveillance personnelcomplete a standardized case reportform that includes information ondemographics, clinical presentation,

vaccination history, andepidemiologic information, includingsource of infant infection (SOI).

Definitions

Cases were defined as those ,1 yearof age on date of cough onset andwere classified according to theCouncil of State and TerritorialEpidemiologists case definition forpertussis that was in place during thestudy period. The clinical casedefinition used for this analysisrequired cough of $2 weeks’duration with at least 1 clinicalsymptom (paroxysms, inspiratorywhoop, or posttussive vomiting).Probable cases were defined as thosepersons meeting the clinical casedefinition. Confirmed cases werepersons who had isolation ofBordetella pertussis from culture anda cough illness of any duration. Caseswere also classified as confirmed ifthey met the clinical case definitionand were either positive bypolymerase chain reaction or hadcontact with a laboratory-confirmedcase of pertussis; cases in persons$11 years of age from Massachusettswith a single acute serumimmunoglobulin G antipertussis toxinantibody level of $20 mg/mL werealso classified as confirmed.19

Confirmed and probable cases wereincluded in our analysis for all statesexcept Massachusetts, where onlyconfirmed cases were reported.

The SOI was collected at time ofinterview of the case-patient’s parentor guardian and was defined asa person with cough illness consistentwith pertussis who had contact withthe infant case-patient in the 7- to 20-day period before the date of infantcough onset. Infant parents/guardians were asked whetheranother person with cough illnesswas known (source), the relationshipof that source to the case infant, andthe source’s age. When .1 sourcewas identified, information wasrecorded for the source with theearliest cough onset date to identifythe first known exposure to pertussis.

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Immediate family members weredefined as mothers, fathers, andsiblings and extended familymembers included grandparents,aunts/uncles, and cousins. An SOIidentified as a day-care contact couldrepresent another child attendee ofthe day care or an adult caregiver.

Analytic Methods

Disease incidence was calculatedusing observed case counts asnumerators and surveillancepopulation estimates from bridged-race, postcensal population estimatesfrom the National Center for HealthStatistics as denominators. The racialand ethnic distributions of cases, aswell as the proportion of caseshospitalized, or who died during theirpertussis illness, were calculatedfrom those with a known response;race (black, white, and other race)and ethnicity (Hispanic and non-Hispanic) were analyzed separately.Pearson’s x2 or Fischer’s exact testswere used for the comparison ofproportions; trends over time wereassessed using the x2 linearity testand test for trend. Trends in annualmedian age over time were assessedusing the Jonckheere-Terpstra test.Additionally, to further understandchanges in the age of identified SOIsover time, we compared SOI agedistributions between 2006 and 2009and 2010 and 2013. This breakpointwas used to mirror the changingepidemiology of pertussis in theUnited States and the increasingburden of disease among olderchildren and adolescents beginning in2010; medians were compared usingthe Wilcoxon Mann-Whitney test.P values of ,.05 were consideredstatistically significant for all tests.

RESULTS

Between 2006 and 2013, a total of1306 cases were identified in infants,1 year of age; ∼24.2% were ,2months of age, and 50.5% were male.Case infants were predominantlywhite (852/1149 [74.2%] with

known race), and 28.9% were ofHispanic ethnicity (344/1191 withknown ethnicity); Hispanic ethnicitywas overrepresented among caseswhen compared with the infantpopulation in the participatingsurveillance areas during the studyperiod (18%). Among our studypopulation, 34.0% (440/1294) of thecase infants were hospitalized, 15.4%(86/559) had pneumonia, and ,1%(2/1274) died during their pertussisillness. The average overall incidenceof pertussis among infants ,1 year ofage was 94.9 of 100 000 population,ranging from a high of 227.4 per100 000 population in 2012 to a lowof 58.0 per 100 000 in 2006 (Fig 1).

Overall, an SOI was identified for 569(43.6%) of the infant cases; 44.1% ofthe parents interviewed were unableto identify an SOI for their infants,and the remaining 12.3% did notprovide a response. Of the infantswith a known SOI, the mostcommonly identified sources weresiblings (35.5%), mothers (20.6%),fathers (10.0%), grandparents(7.6%), aunts/uncles (6.5%), andother source, not specified (6.3%);day-care contacts, cousins, friends,babysitters, nieces/nephews, andunknown source accounted for ,5%each of identified sources. Altogether,immediate family members wereidentified as the source of pertussistransmission for 66.1% of infantcases; immediate plus extendedfamily members were identified as

the source for 85.2% of infant cases.Overall, the most common sourcesidentified were similar by raceand ethnicity, with siblings(32.7%–36.2%) accounting for thegreatest proportion of identified SOIsacross all racial and ethnic groups,followed by mothers (17.2%–21.7%).The only significant differencesidentified was the proportion of SOIsidentified as friends (non-Hispaniccase infants were significantly morelikely than Hispanic case infants tohave a friend identified as an SOI;4.8% vs 0%, P = .004) and thoseidentified as other source, notspecified (black case infants weresignificantly more likely than whitecase infants to have the source ofinfection identified as other source;11.8% vs 4.3%, P = .004).

During the first 2 years of the studyperiod (2006–2007), mothers wereidentified most frequently as thesource of pertussis transmission toinfants. However, a shift to siblingsoccurred in 2008, and with theexception of 2009, this predominancecontinued through 2013 (Fig 2). Theproportion of mothers identifiedas the SOI declined significantlyduring the study period (P = .0014),whereas the proportion of siblingSOIs increased (P = .0333); no othersignificant trends were observedamong the other identified SOIs(Fig 2).

Overall, the median age of theidentified SOIs was 14 years (480 of

FIGURE 1Annual pertussis incidence among infants ,1 year of age and number of reported infant cases byEPS site and year, 2006–2013.

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569 with known age; range: 0–74years; Table 1). Although not steadilydecreasing, there was a borderlinesignificant trend in the annual medianage of SOIs over time (P = .0537). Whenthe years were grouped according tothe changing epidemiology of pertussisin the United States, a significantdecrease in median age was observedwhen we compared 2006–2009 (18years of age) to 2010–2013 (12 years ofage; P = .0160). Among sibling sources,the overall median age during the studyperiod was 8 years of age, andfluctuated between a high of 9 years ofage in 2008, to a low of 4.5 years of agein both 2009 and 2013; no significanttrend in sibling age was observed overtime (P = .2202) or when comparingthe 2 time periods (8 years in2006–2009 and 7 years in 2010–2013,P = .9855).

Younger infant age was significantlyassociated with the identification of

a source of infection; 54.1% of infants0 to 1 month of age had a sourceidentified compared with 40.2% ofinfants 2 to 11 months of age(P , .001). Additionally, hospitalizedinfant cases were more likely to havea source of infection identified thanthose not hospitalized for theirpertussis infection (51.6% vs 39.8%,respectively, P , .001); however,when stratified by infant age group,hospitalization was only significantlyassociated with the identification ofan SOI for infants 2 to 11 months ofage. The proportion of white casesthat had an SOI identified was similarto cases classified as other race(46.0% and 41.8%, respectively;P = .34). However, a significantly higherproportion of sources were identifiedamong white cases when comparedwith black cases (35.4%, P = .02).Council of State and TerritorialEpidemiologists–confirmed cases

were also more likely than casesclassified as probable to havea source of infection identified(44.2% of confirmed cases vs 31.3%of probable cases, P = .04). Nosignificant difference was observedfor ethnicity (45.7% of Hispanic caseshad an SOI identified vs 42.3% ofnon-Hispanic cases; P = .31).

Because younger infant age wasa predictor of whether a source ofinfection was identified, we exploreddifferences in the relationship of thesources identified between the 2infant age groups (Fig 3). Across allSOIs, significant differences betweenthe 2 infant age groups were foundfor mother and day-care contact only.Infants 0 to 1 month of age weresignificantly more likely to acquirepertussis infection from theirmothers (P = .002), whereas infants 2to 11 months of age were more likelyto have day-care contact identified astheir source of infection (P = .003).

DISCUSSION

Consistent with previous studies, ouranalysis of 8 years of enhancedsurveillance data identified an SOI forless than half of reported infantpertussis cases, with a similarproportion of sources identified asfamily members. However, contraryto the published US data, our studyrevealed the emergence of siblings asthe major reservoir of infection andrepresents an important shift in thedynamics of pertussis transmission toyoung infants in the United States.Children 7 to 10 years of age began toemerge as a high-incidence age groupfor pertussis in the United States in2008 and continue to experienceelevated rates of disease, along withadolescents, as aP-vaccinated cohortsage.20 As our data suggest, mothersand fathers still play an importantrole in transmitting disease tounprotected infants, but thetransition to siblings and otherschool-age children as the mainsource of infection is not unexpectedin this era of waning aP immunity and

FIGURE 2Relationship of identified sources of infection, by year, 2006–2013. * Includes day-care contacts,cousins, friends, babysitters, and nieces/nephews, unknown source (n = 1). † P , .05.

TABLE 1 Age Distribution of Identified SOIs, 2006–2013

Source of Infection N % With Known Age Median Age (y) Range (y)

Sibling 202 96 8 1–19Mother 117 85 28 1–43Father 57 72 28 20–51Grandparent 43 67 57 37–74Aunt/uncle 37 76 23.5 5–74Other, not specified 36 86 12 0–52Day care 26 62 5.5 1–44Cousin 26 88 8.5 0–30Friend 17 65 13 1–37Babysitter 4 100 17 10–19Niece/nephew 3 66.7 11.5 6–17Unknown 1 100 3 —

Overall 569 84.4 14 0–74

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an increasing burden of pertussis inthese age groups. Changes in themedian age of the SOIs identified inour analysis mirror the changingepidemiology observed in the UnitedStates.

The Advisory Committee onImmunization Practices (ACIP) hasrecommended 2 strategies to protectyoung infants from pertussis: the“cocooning” strategy, which involvesvaccination of adolescent and adultclose contacts of an infant witha single dose of Tdap, and Tdapvaccination during everypregnancy.4,21 We observed thebeginning of the shift from mothers tosiblings in 2008, 3 years after theintroduction of Tdap in the UnitedStates for routine use amongadolescents and adults. Before thecurrent recommendation for Tdapvaccination during every pregnancy,a postpartum dose of Tdap amongnew mothers and other infantcontacts was the preferred strategyfor preventing infant pertussis.Despite slightly higher Tdap coveragein 2012 among women 18 to 49 yearsof age compared with male adults ofthe same age (18.8% vs 14.7%,P # .0001), Tdap uptake still remainslow among women of childbearingage [CDC’s National Health InterviewSurvey (NHIS), unpublished data].Increasing Tdap coverage among newmothers may be conferring someindirect protection to young infants;however, given the low coverage, theimpact is likely minimal and not

a major contributor to the shift inidentified sources of infection.

Another factor that may be associatedwith the transition away frommothers as the most common SOI isthe age distribution of infant cases. Inour study, the proportion of infantcases ,2 months of age decreasedfrom 36.9% in 2006 to 23.4% in 2013(data not shown). We founda significant association betweenyounger infant age and mothers asthe source of infection; however,infants ,2 months of age and infants2 to 11 months of age had the sameproportion of sibling SOIs identified(Fig 3). Although changes in infantage distribution may be contributingto the transition away from mothers,it does not explain the observed shiftto siblings as the major source ofinfant infection.

In the current setting of waningvaccine-induced immunity after boththe childhood pertussis series andthe Tdap booster vaccine amongaP-vaccinated cohorts, additional dosesof Tdap are unlikely to reduce theoverall burden of pertussis and aretherefore not likely to be routinelyrecommended for the generalpopulation.10–12 Although there ismuch debate around the benefits ofTdap revaccination for subsets of thepopulation, such as infant closecontacts, adult uptake of a single doseremains poor (,15% of adults in2012), and coverage wouldpresumably be lower for subsequentdoses.22 Regardless, as our data

suggest, revaccination of adult cocoonmembers is unlikely to halttransmission of disease to infants ifsiblings are the predominantreservoirs of infection. Additionally,recent studies suggest that aP-vaccinated baboons can be colonizedwith B pertussis and successfullytransmit the organism to cohousedanimals.23 Therefore, even in settingswhere all household contacts are up-to-date with pertussis vaccinations,asymptomatic transmission ofpertussis may occur, further impedingthe success of the cocooningstrategy.23,24 For the cocooningstrategy to be successful, there is alsothe assumption that infants areinfected by close contacts. However,as our analysis and other studies haveshown, a source of infection isidentified less than half the time,suggesting either infection bysomeone outside the household orasymptomatic transmission ofdisease. For these reasons, thecocooning strategy is less than ideal,and strong support of vaccinationduring pregnancy is needed tomaximize the protection of infants inthe first critical months of life.

In contrast to previously publishedUS studies on the infant source ofinfection, our analysis of EnhancedPertussis Surveillance data allowedus to monitor the source of infantinfection in a large sample size overmultiple years. Despite notablestrengths of our study, there weresome challenges to identifying thesource of infant pertussis in ouranalysis of surveillance data.Although .1 person with coughillness may have had contact with aninfant case, we only capturedinformation on the potential sourcewith the earliest cough onset andwere unable to quantify the level ofcontact with the case. Potentialsources who were asymptomatic orhad mild illness without cough mayhave also been missed in our study aswe relied solely on parent reportwithout laboratory testing ofhousehold members or other infant

FIGURE 3Differences in relationship of identified SOIs, by case infant age, 2006–2013.

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contacts; additionally, withoutlaboratory confirmation, we wereunable to determine if B pertussis wasthe actual cause of cough illness inthe identified SOIs. It is alsoimportant to note that although wedid have a large sample size, therewere changes in participating sitesover time, potentially making datafrom the earlier years lessgeneralizable.

CONCLUSIONS

Our analysis of US EnhancedPertussis Surveillance data revealeda shift in the source of infantpertussis infection from mothers tosiblings, mirroring the shiftingepidemiology of pertussis in theUnited States. Continued monitoringof the source of infant infectionthrough surveillance is important,especially as the epidemiology ofpertussis changes. In this era of

resurgent pertussis and widespreadtransmission, the primary focus ofprevention and control strategies is toprotect those at highest risk forsevere disease, with emphasis onyoung infants in the first few monthsof life before immunizations begin.With evidence of waning immunityand possible transmission ofpertussis through subclinicalinfections, the current cocooningstrategy is unlikely to offer sufficientprotection of vulnerable infants.Prevention efforts should thereforefocus on increasing Tdap coverageduring pregnancy because this iscurrently our best strategy forproviding direct protection to theinfant, regardless of the changingsource of infant infection.

ACKNOWLEDGMENTS

Christine Miner, Thomas Clark,Roxanne Ryan, Meghan Barnes, Tracy

Woodall, Paul Cieslak, LauraReynolds, Erinn Sanstead, RachelOstadkar, David Selvage, MarisaBargsten, Brooke Doman, SuzanneMcGuire, Bridget Whitney, NancySpina, Glenda Smith, Jillian Karr, KariBurzlaff, Susan Lett, Molly Crockett,and local and district public healthepidemiologists and nurses from thestates of Colorado, Connecticut,Massachusetts, Minnesota, NewMexico, New York, and Oregon.

ABBREVIATIONS

aP: acellular pertussis vaccineEPS: Enhanced Pertussis

SurveillanceSOI: source of infectionTdap: reduced-dose acellular

pertussis vaccine combinedwith tetanus and diphtheriatoxoids

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2015 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

FUNDING: Enhanced Pertussis Surveillance is supported through a Centers for Disease Control and Prevention cooperative agreement.

POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

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DOI: 10.1542/peds.2015-1120 originally published online September 7, 2015; 2015;136;635Pediatrics 

Kudish, Joan Baumbach, Shelley Zansky, Amanda Faulkner and Stacey W. MartinTami H. Skoff, Cynthia Kenyon, Noelle Cocoros, Juventila Liko, Lisa Miller, Kathy

Sources of Infant Pertussis Infection in the United States

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DOI: 10.1542/peds.2015-1120 originally published online September 7, 2015; 2015;136;635Pediatrics 

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Sources of Infant Pertussis Infection in the United States

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ISSN: 1073-0397. 60007. Copyright © 2015 by the American Academy of Pediatrics. All rights reserved. Print the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois,has been published continuously since 1948. Pediatrics is owned, published, and trademarked by Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it

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